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Neuroendocrine Regulation of Appetitive Ingestive Behavior

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Neuroendocrine Regulation of Appetitive Ingestive Behavior View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Frontiers - Publisher Connector REVIEW ARTICLE published: 15 November 2013 doi: 10.3389/fnins.2013.00213 Neuroendocrine regulation of appetitive ingestive behavior Erin Keen-Rhinehart 1*, Katelynn Ondek 1 and Jill E. Schneider 2 1 Department of Biology, Susquehanna University, Selinsgrove, PA, USA 2 Department of Biological Sciences, Lehigh University, Bethlehem, PA, USA Edited by: Food availability in nature is often irregular, and famine is commonplace. Increased Alfonso Abizaid, Carleton University, motivation to engage in ingestive behaviors increases the chance of survival, providing Canada additional potential opportunities for reproduction. Because of the advantages conferred Reviewed by: by entraining ingestive behavior to environmental conditions, neuroendocrine mechanisms Hélène Volkoff, Memorial University of Newfoundland, Canada regulating the motivation to acquire and ingest food have evolved to be responsive to Tatsushi Onaka, Jichi Medical exogenous (i.e., food stored for future consumption) and endogenous (i.e., body fat University, Japan stores) fuel availability. Motivated behaviors like eating occur in two phases. The appetitive *Correspondence: phase brings animals into contact with food (e.g., foraging, food hoarding), and the Erin Keen-Rhinehart, Department of more reflexive consummatory phase results in ingestion (e.g., chewing, swallowing). Biology, Susquehanna University, 514 University Ave., Selinsgrove, PA Quantifiable appetitive behaviors are part of the natural ingestive behavioral repertoire 17870, USA of species such as hamsters and humans. This review summarizes current knowledge e-mail: [email protected] about neuroendocrine regulators of ingestive behavior, with an emphasis appetitive behavior. We will discuss hormonal regulators of appetitive ingestive behaviors, including the orexigenic hormone ghrelin, which potently stimulates foraging and food hoarding in Siberian hamsters. This section includes a discussion of the hormone leptin, its relation to endogenous fat stores, and its role in food deprivation-induced increases in appetitive ingestive behaviors. Next, we discuss how hormonal regulators interact with neurotransmitters involved in the regulation of ingestive behaviors, such as neuropeptide Y (NPY), agouti-related protein (AgRP) and α-melanocyte stimulating hormone (α-MSH), to regulate ingestive behavior. Finally, we discuss the potential impact that perinatal nutrient availability can have on the neuroendocrine regulation of ingestive behavior. Understanding the hormonal mechanisms that connect metabolic fuel availability to central appetite regulatory circuits should provide a better understanding of the neuroendocrine regulation of the motivation to engage in ingestive behavior. Keywords: food hoarding, leptin, ghrelin, neuropeptide Y, maternal effects, gestational programming, hypothalamus, obesity INTRODUCTION humans inhabit an environment with an overabundance of highly Although obesity was rare in the human population for thou- palatable, easily accessible food sources, transforming these once sands of years (Haslam, 2007), it is now one of the leading health beneficial adaptations into health liabilities. Therefore, under- issues worldwide and has been declared a global epidemic by the standing the basic neuroendocrine regulation of food and body World Health Organization (Caballero, 2007). Despite concerted fat storage and the mechanisms underlying the adaptations to efforts to solve this problem, obesity rates continue to rise world- a food-insecure environment is a central issue to understanding wide. To understand human ingestive behavior and the origins and combating the obesity epidemic (Ulijaszek, 2002). of this epidemic, it is useful to consider an evolutionary per- Human obesity studies typically focus on metabolism, adi- spective (Bronson, 1989; Neel, 1999; Prentice, 2005; Schneider, pogenesis, and meal patterns. Human foraging and hoarding 2006). Fluctuating food supply and famine have been a consistent behavior typically is dismissed as irrelevant to understanding threat to survival for most animals, including humans (Prentice, the health issues surrounding overeating, obesity, and diabetes. 2005). Selection pressures resulting from these fluctuations favor Some data is available, however, on food purchasing behavior, the ability to store energy sources on the body as fat and/or and these studies indicated that 85% of the energy content of the propensity to store food in the home. These abilities pro- the human diet consists of food purchased for consumption at vide a buffer against a variable or unpredictable food supply, and home (Ransley et al., 2003). These types of studies also con- thus allow animals to optimize reproductive success (Prentice, firm the well-known anecdote that purchasing food when food 2005; Schneider, 2006). These phenotypic properties are phys- deprived or “hungry” increases food purchasing, (Dodd et al., iologic (turning off unnecessary functions), metabolic (slowing 1977; Tom, 1983). In addition, obese individuals are likely to basal metabolic rate), behavioral (binge eating, food hoarding, purchase more food per person and more calorically dense food decreased physical activity), and adipogenic (generation of inter- (Ransley et al., 2003; Epstein et al., 2007). After foraging for food nal fat stores, (Prentice, 2005). In western, industrialized societies, at the grocery store, humans then store the food at home for www.frontiersin.org November 2013 | Volume 7 | Article 213 | 1 Keen-Rhinehart et al. Neuroendocrine regulation of appetitive ingestive behavior future consumption in freezers and pantries (a.k.a. hoarding). Adrenal steroids (Stevenson and Franklin, 1970), and other pro- Efforts to understand the neuroendocrine differences responsible teins and peptides of the hypothalamic-pituitary-adrenal (HPA) for these incongruities between the behaviors of lean and obese axis significantly impact food intake (reviewed by Heinrichs and individuals have employed a variety of animal models. Richard, 1999; Bergonzelli et al., 2001). In addition, estradiol, Food intake is the most studied ingestive behavior, but other testosterone, progesterone, and other neuroendocrine factors of ingestive behaviors are likely to be important. In the long his- the hypothalamic-pituitary-gonadal axis (HPG) axis affect food tory of research in behavioral endocrinology, motivated behavior intake (reviewed by Wade, 1976; Schneider and Wade, 1999; is thought to be comprised of two main phases: the appetitive Schneider et al., 2002). Finally, the metabolic hormones, leptin, and the consummatory phases (Craig, 1918). Appetitive behav- insulin, glucagon, ghrelin, and glucagon-like peptide-I (GLP-I), iors are flexible, non-stereotyped responses that bring an animal as well as central factors, such as neuropeptide Y (NPY), agouti- into contact with a goal object, whereas consummatory behav- related protein (AgRP), cocaine and amphetamine-regulated iors are the final reflexive, stereotyped responses after decisions transcript (CART) and the melanocortins reliably affect consum- and efforts have been made to reach the goal object. Both appet- matory ingestive behavior in laboratory animals (reviewed by itive and consummatory behaviors can increase with hunger and Barsh and Schwartz, 2002; Zigman and Elmquist, 2003; Schwartz the desire immediately to consume food and to store energy. and Porte, 2005). Most recently, there has also been a push to Eaten food can be stored on the body as adipose tissue depots, understand the role of reward circuits and dopamine in the regu- while hoarded food is stored in the home or burrow for later lation of ingestive behavior (Abizaid et al., 2006b; Hommel et al., consumption during energetic deficits. The important distinc- 2006; Abizaid, 2009). We shall attempt to review the contributions tion lies in the fact that consummatory behaviors also reflect the of each of these three systems to the neuroendocrine regulation of ability to perform motor actions. Therefore, measures of food consummatory ingestive behavior. intake can be confounded by limits on the ability of the ani- mal to eat or digest food, or by many other postingestional cues. THE ARCUATE PERSPECTIVE ON THE REGULATION OF By contrast, appetitive behaviors are a more “pure” reflection of CONSUMMATORY INGESTIVE BEHAVIOR motivation for acquiring fuels either for eating or calorie storage. The often co-localized orexigenic neuropeptides AgRP and NPY Some appetitive ingestive behaviors occur at different times than are the major products of the Arc that stimulate food intake consummatory behaviors, and appetitive behaviors most useful (Kalra et al., 1999; Morton and Schwartz, 2001; Ellacott and Cone, for scientific study are those that can occur even in the absence of 2004). The anorexigenic neuropeptide α-melanocyte stimulat- changes in food intake (Bartness and Clein, 1994; Bartness, 1997; ing hormone (α-MSH), a cleavage product of the proopiome- Buckley and Schneider, 2003). For example, hungrier animals lanocortin (POMC) gene, and CART are thought to oppose the initiate meals sooner, avidly consume an unpalatable substance, effects of NPY and AgRP (reviewed by Zigman and Elmquist, make more effort to gain access to food, and hoard more food in 2003; Schwartz and Porte, 2005). According to the Arc perspec- their home or burrow (reviewed by Keen-Rhinehart et al., 2010; tive, anorexigenic
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